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CRISPR, adaptive immunity system in Archaea and Bacteria: Lamarckian evolution and a general model of evolution of environmental sensors
Speaker: Eugene V. Koonin , National Center for Biotechnology Information, National Library of Medicine, National Institutes of
The CRISPR-Cas adaptive immunity system is present in nearly all Archaea and about half of Bacteria. This system consists of arrays of Clustered Regularly Interspaced Short Palindromic Repeats (CRISPR) and suits of CRISPR-Associated (cas) genes; the CRISPR cassettes contains unique spacers about 40 basepairs in length within each repeat unit. Some of the spacers are identical to fragments of viral or plasmid genes. It has been shown that Cas proteins provide enzymatic activities that are required for utilization of the spacer transcripts as guide RNAs to cleave and inactivate the cognate alien DNA and in some cases possibly mRNA. The CRISPR-Cas systems are encoded by operons that have extraordinarily diverse architectures and a high rate of evolution of both the cas genes and the unique spacer content. Three complementary approaches to the study of CRISPR evolution will be presented. First, comprehensive analysis of the sequences and structures of Cas proteins using the most sensitive methods of computational analysis yielded a simple scenario for the origin and evolution of the CRISPR-Cas systems that implies the origin of prokaryotic adaptive immunity in thermophilic Archaea. Second, a comprehensive analysis of the selection processes that act on cas genes revealed a gradient from moderate to extremely weak purifying selection across the cas gene suite. Third, a mathematical model based on a cost-benefit analysis of the CRISPR-Cas system in the course of its coevolution with viromes of varying diversity was developed. Exploration of the parameter space of this model shows that selection prevents the loss of the CRISPR-Cas system within an interval of moderate viral diversity. At both very low and very high viral diversity, CRISPR-Cas systems become practically useless for bacteria and archaea, and are lost due to their intrinsic cost. This model has more general applications for the evolution of various environmental sensors. The CRISPR-Cas systems that incorporate new information into a genome in response to environmental cues seem to present a case of bona fide Lamarckian evolution.